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The Paradox of the Plankton G. E. Hutchinson the American The Paradox of the Plankton G. E. Hutchinson The American Naturalist, Vol. 95, No. 882. (May - Jun., 1961), pp. 137-145. Stable URL: http://links.jstor.org/sici?sici=0003-0147%28196105%2F06%2995%3A882%3C137%3ATPOTP%3E2.0.CO%3B2-6 The American Naturalist is currently published by The University of Chicago Press. Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/about/terms.html. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/journals/ucpress.html. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. The JSTOR Archive is a trusted digital repository providing for long-term preservation and access to leading academic journals and scholarly literature from around the world. The Archive is supported by libraries, scholarly societies, publishers, and foundations. It is an initiative of JSTOR, a not-for-profit organization with a mission to help the scholarly community take advantage of advances in technology. For more information regarding JSTOR, please contact [email protected]. http://www.jstor.org Mon Jul 2 14:28:26 2007 Vol. XCV, No. 882 The American Naturalist May-June, 1961 THEPARADOXOF THEPLANKTON* G. E. HUTCHINSON Osborn Zoological Laboratory, New Haven, Connecticut The problem that I wish to discuss in the present contribution is raised by the very paradoxical situation of the plankton, particularly the phyto- plankton, of relatively large bodies of water. We know from laboratory experiments conducted by many workers over a long period of time (summary in Provasoli and Pintner, 1960) that most mem- bers of the phytoplankton are phototrophs, able to reproduce and build up populations in inorganic media containing a source of CO,, inorganic nitro- gen, sulphur, and phosphorus compounds and a considerable number of other elements (Na, K, Mg, Ca, Si, Fe, Mn, B, Cl, Cu, Zn, Mo, Co and V) most of which are required in small concentrations and not all of which are known to be required by all groups. In addition, a number of species are known which require one or more vitamins, namely thiamin, the cobalamines (B,, or re- lated compounds), or biotin. The problem that is presented by the phytoplankton is essentially how it is possible for a number of species to coexist in a relatively isotropic or unstructured environment all competing for the same sorts of materials. The problem is particularly acute because there is adequate evidence from en- richment experiments that natural waters, at least in the summer, present an environment of striking nutrient deficiency, so that competition is likely to be extremely severe. According to the principle of competitive exclusion (Hardin, 1960) known by many names and developed over a long period of time by many investi- gators (see Rand, 1752; Udvardy, 1757; and Hardin, 1960, for historic re- views), we should expect that one species alone would outcompete all the others so that in a final equilibrium situation the assemblage would reduce to a population of a single species. The principle of competitive exclusion has recently been under attack from a number of quarters. Since the principle can be deduced mathemati- cally from a relatively simple series of postulates, which with the ordinary postulates of mathematics can be regarded as forming an axiom system, it follows that if the objections to the principle in any cases are valid, some or all the b'iological axioms introduced are in these cases incorrect. Most objections to the principle appear to imply the belief that equilibrium under a given set of environmental conditions is never in practice obtained. Since the deduction of the principle implies an equilibrium system, if such sys- 'Contribution to a symposium on Modern Aspects of Population Biology. Pre- sented at the meeting of the American Society of Naturalists, cosponsored by the American Society of Zoologists, Ecological Society of America and the Society for the Study of Evolution. American Association for the Advancement of Science, New York, N. Y., December 27, 1960. 138 THE AMERICAN NATURALIST tems are rarely if ever approached, the principle though analytically true, is at first sight of little empirical interest. The mathematical procedure for demonstrating the truth of the principle involves, in the elementary theory, abstraction from time. It does, however, provide in any given case a series of possible integral paths that the popu- lations can follow, one relative to the other, and also paths that they cannot follow under a defined set of conditions. If the conditions change the inte- gral paths change. Mere failure to obtain equilibrium owing to external vari- ation in the environment does not mean that the kinds of competition de- scribed mathematically in the theory of competitive exclusion are not oc- curing continuously in nature. Twenty years ago in a Naturalists' Symposium, I put (Hutchinson, 1941) forward the idea that the diversity of the phytoplankton was explicable pri- marily by a permanent failure to achieve equilibrium as the relevant external factors changed. I later pointed out that equilibrium would never be ex- pected in nature whenever organisms had reproductive rates of such a kind that under constant conditions virtually complete competitive replacement of one species by another occurred in a time (t,), of the same order, as the time (t,) taken for a significant seasonal change in the environment. Note that in any theory involving continuity, the changes are asymptotic to com- plete replacement. Thus ideally we may have three classes of cases: 1. t, << t,, competitive exclusion at equilibrium complete before the environment changes significantly. 2. t, 2 t, , no equilibrium achieved. 3. t, >> t,, competitive exclusion occurring in a changing environment to the full range of which individual competitors would have to be adapted to live alone. The first case applies to laboratory animals in controlled conditions, and conceivably to fast breeding bacteria under fairly constant conditions in nature. The second case applies to most organisms with a generation time approximately measured in days or weeks, and so may be expected to occur in the plankton and in the case of populations of multivoltine insects. The third case applies to animals with a life span of several years, such as birds and mammals. Very slow and very fast breeders thus are likely to compete under condi- tions in which an approach to equilibrium is possible; organisms of inter- mediate rates of reproduction may not do so. This point of view was made clear in an earlier paper (Hutchinson, 1953), but the distribution of that pa- per was somewhat limited and it seems desirable to emphasize the matter again briefly. It is probably no accident that the great proponents of the type of theory involved in competitive exclusion have been laboratory workers on the one hand (for example, Gause, 1934, 1935; Crombie, 1947; and by implication Nicholson, 1933, 1957) and vertebrate field zoologists (for example, Grin- nell, 1904; Lack, 1954) on the other. The major critics of this type of ap- PARADOX OF THE PLANKTON 139 proach, notably Andrewartha and Birch (1954), have largely worked with in- sects in the field, often under conditions considerably disturbed by human activity. DISTRIBUTION OF SPECIES AND INDIVIDUALS MacArthur (1957, 1960) has shown that by making certain reasonable as- sumptions as to the nature of niche diversification in homogeneously diver- sified' biotopes of large extent, the distribution of species at equilibrium follows a law such that the rth rarest species in a population of Ss species and N, individuals may be expected to be This distribution, which is conveniently designated as type I, holds remark- ably well for birds in homogeneously diverse biotopes (MacArthur, 1957, 1960), for molluscs of the genus Conus (Kohn, 1959, 1960) and for at least one mammal population (J. Armstrong, personal communication). It does not hold for bird faunas in heterogeneously diverse biotopes, nor for diatoms settling on slides (Patrick in MacArthur, 1960) nor for the arthropods of soil (Hairston, 1957). Using Foged's (19.54) data for the occurrence of plank- tonic diatoms in Braendegird S# on the Danish island of Funen, it is also apparent (figure 1) that the type I distribution does not hold for such assem- blages of diatom populations under quite natural conditions either. MacArthur (1957, 1960) has deduced two other types of distribution (type I1 and type 111) corresponding to different kinds of biological hypotheses. These distributions, unlike type I, do not imply competitive exclusion. So far in nature only type I distributions and a kind of empirical distribution which I shall designate type IV are known. The type IV distribution given by dia- toms on slides, in the plankton and in the littoral of Braendegdrd S6, as well as by soil arthropods, differs from the type I in having its commonest species commoner and all other species rarer. It could be explained as due to het- erogeneous diversity, for if the biotope consisted of patches in each one of which the ratio of species to individuals differed, then the sum of the as- semblages gives such a curve. This is essentially the same as Hairston's (1959) idea of a more structured community in the case of soil arthropods than in that of birds.
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